Circular genetic structure of the Abies nephrolepis species complex shaped by the circular landform of Northeast Asia

Aim: Pinaceae have been noted for their tendency towards reticulation as a
result of interspecific hybridization. Here, we demonstrated the
phylogeographic dynamics of the native Northeast Asian sub-alpine conifer,
Abies nephrolepis species complex (ANSC), evolving in circular overlaps
along the Northeast Asian landform, which functions as a corridor with the
sea, thus acting as a geographic barrier. Location: Northeast Asia: the
Korean Peninsula, Japanese Archipelago, Russian Far East, and northeastern
China Taxon: Abies nephrolepis species complex (Family Pinaceae, Genus
Abies, Section Balsamea, Abies nephrolepis, A. koreana, A. veitchii, and
A. sachalinensis) Methods: A total of 728 individuals from 38 ANSC
populations were analysed using multiplexed inter-simple sequence repeat
genotyping by sequencing to capture variations in bi-parental nuclear
genomes. Eight mitochondrial regions and eight chloroplast regions of each
individual were sequenced using the MiSeq platform and Sanger sequencing.
Species distribution models were generated. Results: Bayesian clustering
with 507 nuclear single nucleotide polymorphisms and the discrepancy
between cytoplasmic and nuclear genome lineages implied contemporary and
ancient connections between neighbouring species in the form of circular
overlap. This genetic connectivity was supported by principal component
analysis. Strong correlations between genetic distance and geographic
distance were observed, suggesting that gene flow occurs through a
continuous chain around the sea. We also found that gene flow direction
and intensity changed over time, with support from paleodistribution
modelling. Conclusion: Past hybridization events were captured in
cytoplasmic genomes, generating heterogeneity across maternal ancestries.
This intensive phylogeographic study demonstrates speciation with
incomplete reproductive isolation (continuous gene flow) among
neighbouring species with an alteration of the direction and intensity of
gene flow due to climate change. The divergence of ANSC due to repeated
isolation and reconnection caused by heterogenous physiological
environments and climate fluctuation provides a model to solve
evolutionary scenarios for reticulate evolution in Pinaceae and other
plants.